Outdoor biting behaviour and insecticide resistance in malaria vectors

might challenge malaria elimination in Southern Province, Zambia Javan Chanda1

, Kochelani Saili1, Christopher Lungu1, Chadwick Sikaala2, John Miller 1 1PATH Malaria Control and Elimination Partnership in Africa (MACEPA); 2Government of the Republic of Zambia, Ministry of Health, National Malaria Elimination Centre

Background In the last decade, malaria has been reduced in Africa by

33% as a result of the rapid roll-out of malaria control interventions (WHO, 2011).

In Zambia, long-lasting insecticide-treated nets (LLINs) and indoor residual spraying (IRS) are the main malaria vector control interventions.

The use of these interventions depends on high coverage, vector susceptibility status to insecticides, and the indoor biting and resting behaviour of malaria vectors.

However, there is limited information on the behaviour of malaria vectors and their susceptibility to insecticides used for vector control in Zambia’s Southern Province.

This study aimed to monitor vector behaviour, species vector composition, and vector susceptibility to insecticides used for malaria vector control in Southern Province to guide the malaria elimination agenda.

Methods

Indoor, host-seeking mosquitoes were collected from 36 randomly selected houses from April to May 2015 and from November to December 2015 using Human Landing Catches, a method used to collect live mosquitoes attempting to bite human baits both inside and outside a house.

Three pairs of human landing collectors were recruited and trained in 12 study areas on how to collect mosquitoes. Mosquito collection was conducted on an hourly basis starting from 18:00 and ending at 06:00 for 15 consecutive days. Individual mosquito collectors were given one tablet of deltaprim™ once a week as a prophylactic drug.

Insecticide susceptibility tests were conducted on 0.05% deltamethrin, 0.1% bendiocarb, 4% DDT, and 0.25% pirimiphos-methyl following the WHO standard protocol. Metabolic resistance was determined in populations of An. gambiae s.l and An. funestus by using a synergist piperonyl butoxide (PBO).

Multiplex Polymerase Chain Reaction (PCR) was used to determine sibling species of An.gambiae s.l and Anopheles funestus.

Results continued

Standard WHO bioassays indicate that populations of An. arabiensis are resistant to deltamethrin; mortality rates ranged from 78% to 95% (Figure 4).

In An. funestus, high resistance was detected to deltamethrin (mortality rates ranged from 14% to 42%) and bendiocarb (mortality rates ranged from 41% to 56%).

In all the study sites, An. arabiensis and An. funestus recorded 100% susceptibility to DDT and pirimiphos-methyl.

Pre-exposure of An. arabiensis and An. funestus to

piperonyl butoxide nullified both pyrethroid and carbamate

resistance.

Figure 4. WHO bioassays of malaria vectors in the study areas of Southern Province

Results

A total of 5,509 adult Anopheles mosquitoes were collected from Apr–May 2015 and Nov–December 2015.

72 % (n= 3966) constituted An. gambiae s.l, 18% (n= 991) constituted An. funestus, and 2% (n = 113) were other anopheline mosquitoes (summarized in Figure 2).

PCR confirmed the presence of An. arabiensis, An. quadriannulatus, and An. funestus s.s in the study sites.

An. arabiensis mainly bit humans outdoors (0.55) rather than indoors (0.45), (ANOVA: F=7.1294, df=11, P= 0.0217). In contrast, An. funestus mainly bit humans indoors (0.55) rather than outdoors (0.45), ANOVA: F=6.55, P=0.03.

1426 Government of the

Republic of Zambia

Figure 1. Map of Zambia showing study sites in Southern Province

Figure 2. Vector species composition in the study areas of

Southern Province

Figure 3. Biting behaviour of Anopheles arabiensis and funestus in the study

areas of Southern Province

Conclusions

The outdoor, early-biting behaviour of malaria vectors in the study areas can reduce the effectiveness of LLINs and IRS for malaria control and elimination in Southern Province.

The high pyrethroid and carbamate resistance in populations of An. arabiensis and An. funestus may threaten the effectiveness of chemical-based malaria vector control interventions (LLINs and IRS) in the study areas.

Persistent outdoor biting behaviour of An. arabiensis coupled with high pyrethroid resistance in An. funestus is likely to undermine malaria elimination efforts by extending residual transmission of malaria in the study areas.

To adequately suppress malaria transmission and attain malaria elimination in the study areas, additional interventions that target outdoor-biting mosquitoes and sustainable insecticide resistance management strategies are likely to be required in Southern Province, Zambia.